ORIGINAL ARTICLE
Long-term Follow-up Study of Radial Forearm Free Flap Reconstruction After Hemiglossectomy Masaya Akashi, DDS, PhD,* Kazunobu Hashikawa, MD, PhD,† Akiko Sakakibara, DDS, PhD,* Takahide Komori, DDS, PhD,* and Hiroto Terashi, MD, PhD† Abstract: Previous studies on postoperative long-term results in patients who underwent reconstructive free flap transfer following hemiglossectomy had some issues, including the heterogeneity of the patient population and the observation period. The present study aimed to evaluate changes of reconstructed tongues in patients who underwent radial forearm free flap (RFFF) after hemiglossectomy with long-term follow-up. We enrolled 23 patients who underwent RFFF after hemiglossectomy with a postoperative follow-up of 5 years or more. Postoperative status (eating, speech, sensation function) was assessed by concise medical inquiries. Morphological changes of flaps were evaluated by reviewing clinical photographs. Hemiglossectomy involving the base of the tongue was performed in 4 cases (17.4%) and was limited to the mobile tongue in 19 cases (82.6%). The mean follow-up was 85.4 months (range, 60–122 months). All patients experienced gradually improved postoperative status. The most significant improvement was found between 1 and 5 years after surgery (P = 0.007), but not between 1 and 3 years (P = 0.075) or between 3 and 5 years (P = 0.530). In almost all of the flaps, there were few morphological changes throughout the follow-up period. Postoperative status in patients who underwent reconstructive RFFF following hemiglossectomy improved sequentially. Key Words: Tongue cancer, Hemiglossectomy, Radial forearm free flap, Postoperative status, Long-term follow-up (J Craniofac Surg 2015;26: 44–47)
surgery remains one of the important challenges of head and neck surgery. Surgical treatment of primary lesions of the tongue can be clinically classified into 4 groups: partial, hemi, subtotal, and total glossectomy. The severity of the postoperative functional impairment depends on the degree of the resection.1 The shape and bulk of the reconstructed tongue after subtotal or total glossectomy are closely correlated with postoperative swallowing capacity and speech.2 Flaps that are excessively bulky limit tongue mobility in patients with anterior tongue defects.3 The thin, pliable radial forearm free flap (RFFF) has shown its superiority in tongue reconstruction, especially for hemiglossectomy defects, because maximizing mobility of the residual tongue is the most critical factor for postoperative function.4 The benefit of RFFF’s bulk, which is necessary for swallowing after intraoral cancer resection, has also been emphasized.5 Some long-term follow-up studies were conducted to address the functional outcome of the neotongue.3,6–9 Despite the importance of those studies, some issues remain, such as the heterogeneity of the study population with its varying factors, including the location of the primary cancer, the extent of the surgical resection, and the observation period. Especially, because the residual tongue following ablation plays important functional roles, the modalities for evaluating the functional outcome in patients who undergo subtotal or total glossectomy should not be applied to those who undergo hemiglossectomy. The purpose of the current study was to evaluate sequential changes of postoperative status including eating, speech, and sensory function in patients who underwent RFFF reconstruction after hemiglossectomy.
T
he tongue is the most common site for primary intraoral cancer. Most tongue cancers are found on the anterior two-thirds of the tongue’s lateral border. Tongue reconstruction following ablative What Is This Box? A QR Code is a matrix barcode readable by QR scanners, mobile phones with cameras, and smartphones. The QR Code links to the online version of the article.
From the Departments of *Oral, Maxillofacial Surgery and †Plastic Surgery, Kobe University Graduate School of Medicine, Kobe, Japan. Received February 14, 2014. Accepted for publication June 20, 2014. Address correspondence and reprint requests to Masaya Akashi, DDS, PhD, Department of Oral and Maxillofacial Surgery, Kobe University Graduate School of Medicine, Kusunoki-cho 7-5-2, Chuo-ku, Kobe 650-0017, Japan; E-mail: [email protected] Ethical approval was provided by the institutional review board of the Kobe University Hospital (protocol no. 1439). No funding was received of this study. The authors report no conflicts of interest. Copyright © 2014 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000001176
44
MATERIALS AND METHODS Patients A total of 57 consecutive patients underwent radial forearm fasciocutaneous free flap reconstruction after ablative surgery for tongue cancer at Kobe University Hospital from August 2002 to December 2007. The criteria for enrollment in this study were patients who had undergone hemiglossectomy and a follow-up of 5 years or more postoperatively with regular follow-up visits. Of the 57 patients, 34 were excluded because their glossectomy had been subtotal or total, they had a history tumor recurrence after surgery, or there was an absence of regular follow-up visits. Epidemiological data were retrospectively gathered from the medical charts: age, sex, histological diagnosis, extent of tongue resection, reconstruction surgical procedures, postoperative ischemic complications, postoperative radiotherapy, and follow-up period. The institutional review board of the Kobe University Hospital approved this retrospective study.
Functional Evaluation During the routine follow-up visits, simple medical inquiries about the postoperative status of patients who underwent hemitongue reconstruction yielded a score range of 0 to 6 points. A single plastic surgeon (K.H.) performed almost all of these clinical assessments.
The Journal of Craniofacial Surgery • Volume 26, Number 1, January 2015
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 26, Number 1, January 2015
Radial Forearm Free Flap Reconstruction
9 women (39.1%). Histological diagnosis was squamous cell carcinoma in all cases. Clinical T stages were as follows: T1, 1 (4.3%); T2, 18 (78.3%); T3, 4 (17.4%). Hemiglossectomy involving the base of the tongue was performed in 4 cases (17.4%). It was limited to the mobile tongue in 19 cases (82.6%). A unilobed radial forearm flap was sutured into the residual tongue tip, with microvascular anastomoses of the radial artery, radial vein, and cephalic vein to the recipient vessels without nerve anastomosis in all cases. There were 2 venous thromboses of the microvascular anastomoses (8.7%). These 2 free flaps were salvaged with a reoperation. No patients underwent postoperative radiotherapy. The mean follow-up period was 85.4 months (range, 60–122 months).
Sequential Changes of Postoperative Status and Reconstructed Tongue Morphology
FIGURE 1. Sequential change of postoperative function. Vertical axis (1–100) represents the percentage of cases acquiring eating, speech, and sensory function = 2 points.
A 2-point scale to evaluate eating function was used. Patients who resumed the same form of diet as was consumed preoperatively were given 2 points. Those who resumed consumption of their preoperative diet but had difficulty eating specific foods (eg, meat or noodles), or they took a very long time to eat, were given 1 point. Those who were unable to consume foods that were in their diet preoperatively were given 0 points. Speech function was evaluated on a 2-point scale. Patients who could talk on the telephone were given 2 points. Those who could talk on the telephone but had difficulty speaking certain words (eg, those with alveolar or velar consonants) were given 1 point. Those who could not talk on the telephone were given 0 points. Sensory function was evaluated on a 2-point scale. Patients who had no complaints were given 2 points. Those who had difficulty eating a hot diet or who bit the flap were given 1 point. Those who could not eat a hot diet and often bit the flap were given 0 points. Sequential changes in postoperative status were retrospectively analyzed. We assessed morphological alterations of the reconstructed tongues by reviewing clinical photographs.
Statistical Analysis Fisher exact test was used to identify significant associations among categorical values. Statistical significance was accepted at P < 0.05, and all calculations were performed using SPSS version 15.0 (SPSS, Chicago, IL).
RESULTS
TABLE 2. Associations With Postoperative Status (Over 5 Points) at 5 Years or Greater Postoperatively No. Cases (%)
Postoperative Status ≤5 (%)
Age, y
At the time of surgery, the mean age of the 23 study subjects was 57 years (range, 33–71 years). There were 14 men (60.9%) and TABLE 1. Passage of Time and Their Associations With Postoperative Status (Over 5 Points) No. Cases Acquiring Postoperative Status ⩽5 (%) 3y ≥5 y
DISCUSSION This study investigated the long-term change in the postoperative status of patients who underwent RFFF reconstruction after hemiglossectomy. It revealed sequential improvement. Although previous long-term follow-up studies have assessed functional outcome of the neotongue, there remained some issues, such as the heterogeneity of study population and the duration of the follow-up period. In 1 report, the functional outcomes in patients
Parameter
Population
1y
Postoperative status improved sequentially. At 1 year after surgery, 21 patients (91.3%) could partake of the same type of diet as they had preoperatively, and all patients could talk on the telephone. While eating and speech function gradually improved, the extent of sensory function improvement lagged behind (Fig. 1). Eight patients (34.8%) had difficulty eating a hot diet or had bitten the flap throughout the follow-up period. At 5 years or longer after surgery, 6 patients (26.1%) were given 4 postoperative status points, 8 (34.8%) were given 5 points, and 9 (39.1%) were assigned 6 points. Statistical differences were analyzed between the patients who were given less than 4 points and those who rated more than 5 points. A significant improvement was found between 1 and 5 years after surgery (P = 0.007), but not between 1 and 3 years (P = 0.075) or 3 and 5 years (P = 0.530) (Table 1). No relation was found between age (P = 0.245), sex (P = 0.643), extent of resection (P = 0.270), or venous thrombosis (P = 1.000) (Table 2). Morphological alterations of reconstructed tongues are shown in Figure 2. The furrows in 2 reconstructed tongues gradually disappeared, which probably reflected the sequential decrease in flap volume (Figs. 2A–D). Morphological changes were not recognized in other flaps during the long-term follow-up periods. Representative cases are shown in Figures 2E–H.
7 (30.4) 14 (60.9) 17 (73.9)
P 0.075 0.007 0.530
≤59 ≥60 Sex Male Female Extent of resection Mobile tongue Mobile tongue and base of tongue Venous thrombosis − +
P 0.245
10 (43.5) 13 (56.5)
70.0 76.9
14 (60.9) 9 (39.1)
79.0 66.7
19 (82.6) 4 (17.4)
79.0 50.0
21 (91.3) 2 (8.7)
71.0 100.0
0.643
0.270
1.000
© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
45
Akashi et al
The Journal of Craniofacial Surgery • Volume 26, Number 1, January 2015
FIGURE 2. Long-term morphological alterations in the reconstructed tongue. (A–D) Note that the furrows in the flaps disappeared sequentially. A and B, A 42-year-old man at 3 years after surgery (A) and at 5 years (B). C and D, A 47-year-old woman 1 year after surgery (C) and at 8 years (D). E–H, A 70-year-old man at 2 years after surgery (E) and at 5 years (F). A 63-year-old woman 3 years after surgery (F) and at 7 years (H). They exhibited few flap volume changes during this long-term period.
who underwent free flap reconstruction following hemiglossectomy and subtotal and total glossectomy were evaluated with the same modalities.7 The modalities for evaluating the functional outcome in patients who undergo subtotal or total glossectomy should not be applied to those who undergo hemiglossectomy, because the residual tongue following ablation plays critical roles in postoperative function. Various modalities have been applied to evaluate function of the postoperative tongue in patients who have undergone free flap reconstruction (eg, speech intelligibility assessment by speech therapists, swallowing assessment by video-fluoroscopic images, sensory function assessment by 2-point discrimination test).5,6,10 These studies have provided important information, but the examinations cannot be performed routinely during the practical follow-up of hemiglossectomy patients. We evaluated such patients postoperatively with simple medical inquiries, emphasizing their ability to talk on the telephone, which is thought to reflect patients’ speech function in daily life. Questionnaires about this ability are generally included in the applicable methods to evaluate quality of life (QOL), such as the European Organization for Research and Treatment of Cancer Quality of Life Core Questionnaire and Head and Neck Module.11 We also took into account the ability to partake of the same type of diet as was consumed before the operation. This factor was chosen because eating includes mastication and deglutition, which
46
are influenced by the patient’s age and whether he/she is dentate or edentate. In a previous study, functions that included swallowing were usually at their worst after cancer treatment, although 1 year postoperatively, almost all patients were consuming a socially acceptable diet.12 In our study, a single patient was unable to consume the same diet as before the surgery at 1 year after surgery but experienced improved eating function sequentially during the 5 years postoperatively, as was seen in all of the other patients (Fig. 1). Conversely, all patients could talk on the telephone 1 year after surgery, and speech improvement, based on our assessment modality, was almost complete at 3 years (Fig. 1). Hsiao et al,5 in the comparative study between primary closure and RFFF reconstruction after hemiglossectomy, reported that the nonfunctional flap added bulk, improving pharyngeal clearance by maintaining the tongue-to-mouth roof contact that was necessary for the swallowing process. It also, however, hindered articulation by restricting mobility of the residual tongue. Although our speech assessment may be more lenient than that of Hsiao et al, the ability to talk on the telephone is considered acceptable for the neotongue. Because acquisition of eating function as well as speech function is required for tongue reconstruction, pliable tissue transfer that does not restrict residual tongue mobility is needed. Sequential improvement of postoperative status in our patients was considered to be due to the pliability of the RFFF. We also evaluated the difficulty of consuming a hot diet and flap biting as parameters of sensory impairment. Whereas there was gradual improvement of sensory function during the 5 years after surgery, the percentage of patients given 2 points of sensory function was lower than ones of eating and speech functions. Previous studies revealed that sensory-innervated flaps for intraoral reconstruction allowed better and faster recovery of sensation than noninnervated flaps.13,14 It is also known that noninnervated flaps eventually may recover sensation through peripheral and recipient bed axonal sprouting, although there is no complete recovery over the entire flap.15,16 Loewen et al10 reported that patients who underwent innervated RFFF reconstruction of the tongue were able to identify cold more accurately than hot. A decrease or loss in protective sensation and pain perception on the free flap may cause a burn as well as flap bites. Flap bites might reflect not only sensory impairment but also bulkiness of the flap or disturbed coordination of mastication.17 Some longitudinal studies to measure changes in QOL in patients with head and neck cancer have been carried out. Rogers et al18 reported that patients tended to emphasize speech, chewing, and swallowing more than other evaluation items (including pain and appearance) at 12 months after surgery. Infante-Cossio et al19 performed a long-term prospective study that included QOL data of 69 patients with oral and oropharyngeal carcinoma. Data were obtained prior to treatment and 1 and 3 years after treatment initiation. They noted that most of the parameters worsened significantly after treatment and during the first year and then gradually improved. At 3 years postoperatively, only a few parameters had not returned to the values before beginning treatment. They concluded that most of the benefit with regard to QOL was acquired during the first years because no further dynamic of QOL was found after the first year of treatment because of tolerance mechanisms over the course of the disease.20 On the other hand, Joo et al21 reported a significant positive correlation between postoperative irradiation and RFFF volume changes estimated by computed tomography or magnetic resonance imaging 3 months to 5 years after surgery—but not 3 months to 1 year or 3 months to 3 years. They recommended overcorrection with 40% larger RFFF volume than the actual defect because the computerdetermined postoperative volume changed by 42.7% between 3 months and 5 years. They noted that the percentage volume of the reconstructed radial forearm flap changed by 15.4% to 75.5% between 3 months and 5 years. In our cases, morphological changes © 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 26, Number 1, January 2015
were small except for 2 flaps that exhibited disappearance of the furrows, as shown in Figures 2A–D. The maintenance of flap volume may be explained by the lack of irradiation in all of our patients. Because our study revealed gradual changes in postoperative status, reconstructive surgeons should follow up for as long as possible to evaluate outcomes in their patients who undergo free flap reconstruction. The free anterolateral thigh perforator flap has been considered an alternative to RFFF for head and neck reconstruction. It has become popular nowadays because it leaves less donor-site morbidity.22 Comparison studies between the RFFF and anterolateral thigh flap have been carried out.23–25 Although they found no significant differences in speech or swallowing between the 2 groups, patients with the free anterolateral thigh flaps had better QOL scores, including appearance among others.25 Long-term follow-up regarding changes in the flap volume or sequential atrophy of the free anterolateral thigh flap is reported in a few studies.26 We have used RFFF as a first-choice flap following hemiglossectomy because it is anatomically constant, it has a long vascular pedicle, it is easy to harvest, and (especially) the skin flap has a pliability that cannot be gained from other tissues. Our results, which showed that the postoperative status of patients improved sequentially, certainly reflect the continuous pliability of this flap, which does not limit the mobility of the residual tongue. Based on their experience, Li et al25 recommended that the free anterolateral thigh flap be used for large defects during head and neck reconstruction. There were some limitations of the study. The retrospective nature and small sample size were problematic. Also, technical examinations (eg, functional assessment by a speech therapist, evaluation of swallowing with video fluoroscopy) were not performed. Our assessment of postoperative status in patients who underwent reconstructive free flap transfer after hemiglossectomy comprised the use of questionnaires that were simpler than those previously reported.18–20 Our evaluation modality may be adequate for practical evaluation during routine follow-up of hemiglossectomy patients but not for clinical research. Also, the postoperative status of total glossectomy patients undergoing free flap reconstruction should be evaluated with a more distinctive method because their postoperative functions are worse than those of hemiglossectomy patients. A prospective investigation with the evaluation modality introduced in the present study should be conducted to confirm the validity of free flap reconstruction following hemiglossectomy. ACKNOWLEDGMENTS The authors thank S. Tahara in the Department of Plastic Surgery, Japanese Red Cross Kobe Hospital; S. Yokoo in the Department of Stomatology and Maxillofacial Surgery, Gunma University Graduate School of Medicine; and doctors in the Departments of Oral and Maxillofacial Surgery and Otolaryngology–Head and Neck Surgery, Kobe University Graduate School of Medicine.
REFERENCES 1. Brown JS, Rogers SN, Lowe D. A comparison of tongue and soft palate squamous cell carcinoma treated by primary surgery in terms of survival and quality of life outcomes. Int J Oral Maxillofac Surg 2006;35:208–214 2. Kimata Y, Sakuraba M, Hishinuma S, et al. Analysis of the relations between the shape of the reconstructed tongue and postoperative functions after subtotal or total glossectomy. Laryngoscope 2003;113:905–909 3. Rhemrev R, Rakhorst HA, Zuidam JM, et al. Long-term functional outcome and satisfaction after radial forearm free flap reconstructions of intraoral malignancy resections. J Plast Reconstr Aesthet Surg 2007;60:588–592 4. Urken ML, Biller HF. A new bilobed design for the sensate radial forearm flap to preserve tongue mobility following significant glossectomy. Arch Otolaryngol Head Neck Surg 1994;120:26–31
Radial Forearm Free Flap Reconstruction
5. Hsiao HT, Leu YS, Lin CC. Primary closure versus radial forearm flap reconstruction after hemiglossectomy: functional assessment of swallowing and speech. Ann Plast Surg 2002;49:612–616 6. Joo YH, Hwang SH, Park JO, et al. Functional outcome after partial glossectomy with reconstruction using radial forearm free flap. Auris Nasus Larynx 2013;40:303–307 7. Engel H, Huang JJ, Lin CY, et al. A strategic approach for tongue reconstruction to achieve predictable and improved functional and aesthetic outcomes. Plast Reconstr Surg 2010;126:1967–1977 8. Yun IS, Lee DW, Lee WJ, et al. Correlation of neotongue volume changes with functional outcomes after long-term follow-up of total glossectomy. J Craniofac Surg 2010;21:111–116 9. Hara I, Gellrich NC, Düker J, et al. Evaluation of swallowing function after intraoral soft tissue reconstruction with microvascular free flaps. Int J Oral Maxillofac Surg 2003;32:593–599 10. Loewen IJ, Boliek CA, Harris J, et al. Oral sensation and function: a comparison of patients with innervated radial forearm free flap reconstruction to healthy matched controls. Head Neck 2010;32:85–95 11. Bjordal K, Hammerlid E, Ahlner-Elmqvist M, et al. Quality of life in head and neck cancer patients: validation of the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire–H&N35. J Clin Oncol 1999;17:1008–1019 12. Markkanen-Leppänen M, Isotalo E, Mäkitie AA, et al. Swallowing after free-flap reconstruction in patients with oral and pharyngeal cancer. Oral Oncol 2006;42:501–509 13. Urken ML, Weinberg H, Vickery C, et al. The neurofasciocutaneous radial forearm flap in head and neck reconstruction: a preliminary report. Laryngoscope 1990;100:161–173 14. Katou F, Shirai N, Kamakura S, et al. Intraoral reconstruction with innervated forearm flap: a comparison of sensibility and reinnervation in innervated versus noninnervated forearm flap. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1995;80:638–644 15. Shindo ML, Sinha UK, Rice DH. Sensory recovery in noninnervated free flaps for head and neck reconstruction. Laryngoscope 1995;105:1290–1293 16. Vriens JP, Acosta R, Soutar DS, et al. Recovery of sensation in the radial forearm free flap in oral reconstruction. Plast Reconstr Surg 1996;98:649–656 17. Kapur KK, Garrett NR, Fischer E. Effects of anaesthesia of human oral structures on masticatory performance and food particle size distribution. Arch Oral Biol 1990;35:397–403 18. Rogers SN, Laher SH, Overend L, et al. Importance-rating using the University of Washington quality of life questionnaire in patients treated by primary surgery for oral and oro-pharyngeal cancer. J Craniomaxillofac Surg 2002;30:125–132 19. Infante-Cossio P, Torres-Carranza E, Cayuela A, et al. Impact of treatment on quality of life for oral and oropharyngeal carcinoma. Int J Oral Maxillofac Surg 2009;38:1052–1058 20. Klug C, Neuburg J, Glaser C, et al. Quality of life 2–10 years after combined treatment for advanced oral and oropharyngeal cancer. Int J Oral Maxillofac Surg 2002;31:664–669 21. Joo YH, Hwang SH, Sun DI, et al. Assessment of volume changes of radial forearm free flaps in head and neck cancer: long-term results. Oral Oncol 2011;47:72–75 22. Wei FC, Jain V, Celik N, et al. Have we found an ideal soft-tissue flap? An experience with 672 anterolateral thigh flaps. Plast Reconstr Surg 2002;109:2219–2226; discussion 2227–2230 23. Hsiao HT, Leu YS, Liu CJ, et al. Radial forearm versus anterolateral thigh flap reconstruction after hemiglossectomy: functional assessment of swallowing and speech. J Reconstr Microsurg 2008;24:85–88 24. de Vicente JC, de Villalaín L, Torre A, et al. Microvascular free tissue transfer for tongue reconstruction after hemiglossectomy: a functional assessment of radial forearm versus anterolateral thigh flap. J Oral Maxillofac Surg 2008;66:2270–2275 25. Li W, Xu Z, Liu F, et al. Vascularized free forearm flap versus free anterolateral thigh perforator flaps for reconstruction in patients with head and neck cancer: assessment of quality of life. Head Neck 2013;35:1808–1813 26. Yamaguchi K, Kimata Y, Onoda S, et al. Quantitative analysis of free flap volume changes in head and neck reconstruction. Head Neck 2012;34:1403–1407
© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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Long-term Follow-up Study of Radial Forearm Free Flap Reconstruction After Hemiglossectomy Masaya Akashi, DDS, PhD,* Kazunobu Hashikawa, MD, PhD,† Akiko Sakakibara, DDS, PhD,* Takahide Komori, DDS, PhD,* and Hiroto Terashi, MD, PhD† Abstract: Previous studies on postoperative long-term results in patients who underwent reconstructive free flap transfer following hemiglossectomy had some issues, including the heterogeneity of the patient population and the observation period. The present study aimed to evaluate changes of reconstructed tongues in patients who underwent radial forearm free flap (RFFF) after hemiglossectomy with long-term follow-up. We enrolled 23 patients who underwent RFFF after hemiglossectomy with a postoperative follow-up of 5 years or more. Postoperative status (eating, speech, sensation function) was assessed by concise medical inquiries. Morphological changes of flaps were evaluated by reviewing clinical photographs. Hemiglossectomy involving the base of the tongue was performed in 4 cases (17.4%) and was limited to the mobile tongue in 19 cases (82.6%). The mean follow-up was 85.4 months (range, 60–122 months). All patients experienced gradually improved postoperative status. The most significant improvement was found between 1 and 5 years after surgery (P = 0.007), but not between 1 and 3 years (P = 0.075) or between 3 and 5 years (P = 0.530). In almost all of the flaps, there were few morphological changes throughout the follow-up period. Postoperative status in patients who underwent reconstructive RFFF following hemiglossectomy improved sequentially. Key Words: Tongue cancer, Hemiglossectomy, Radial forearm free flap, Postoperative status, Long-term follow-up (J Craniofac Surg 2015;26: 44–47)
surgery remains one of the important challenges of head and neck surgery. Surgical treatment of primary lesions of the tongue can be clinically classified into 4 groups: partial, hemi, subtotal, and total glossectomy. The severity of the postoperative functional impairment depends on the degree of the resection.1 The shape and bulk of the reconstructed tongue after subtotal or total glossectomy are closely correlated with postoperative swallowing capacity and speech.2 Flaps that are excessively bulky limit tongue mobility in patients with anterior tongue defects.3 The thin, pliable radial forearm free flap (RFFF) has shown its superiority in tongue reconstruction, especially for hemiglossectomy defects, because maximizing mobility of the residual tongue is the most critical factor for postoperative function.4 The benefit of RFFF’s bulk, which is necessary for swallowing after intraoral cancer resection, has also been emphasized.5 Some long-term follow-up studies were conducted to address the functional outcome of the neotongue.3,6–9 Despite the importance of those studies, some issues remain, such as the heterogeneity of the study population with its varying factors, including the location of the primary cancer, the extent of the surgical resection, and the observation period. Especially, because the residual tongue following ablation plays important functional roles, the modalities for evaluating the functional outcome in patients who undergo subtotal or total glossectomy should not be applied to those who undergo hemiglossectomy. The purpose of the current study was to evaluate sequential changes of postoperative status including eating, speech, and sensory function in patients who underwent RFFF reconstruction after hemiglossectomy.
T
he tongue is the most common site for primary intraoral cancer. Most tongue cancers are found on the anterior two-thirds of the tongue’s lateral border. Tongue reconstruction following ablative What Is This Box? A QR Code is a matrix barcode readable by QR scanners, mobile phones with cameras, and smartphones. The QR Code links to the online version of the article.
From the Departments of *Oral, Maxillofacial Surgery and †Plastic Surgery, Kobe University Graduate School of Medicine, Kobe, Japan. Received February 14, 2014. Accepted for publication June 20, 2014. Address correspondence and reprint requests to Masaya Akashi, DDS, PhD, Department of Oral and Maxillofacial Surgery, Kobe University Graduate School of Medicine, Kusunoki-cho 7-5-2, Chuo-ku, Kobe 650-0017, Japan; E-mail: [email protected] Ethical approval was provided by the institutional review board of the Kobe University Hospital (protocol no. 1439). No funding was received of this study. The authors report no conflicts of interest. Copyright © 2014 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000001176
44
MATERIALS AND METHODS Patients A total of 57 consecutive patients underwent radial forearm fasciocutaneous free flap reconstruction after ablative surgery for tongue cancer at Kobe University Hospital from August 2002 to December 2007. The criteria for enrollment in this study were patients who had undergone hemiglossectomy and a follow-up of 5 years or more postoperatively with regular follow-up visits. Of the 57 patients, 34 were excluded because their glossectomy had been subtotal or total, they had a history tumor recurrence after surgery, or there was an absence of regular follow-up visits. Epidemiological data were retrospectively gathered from the medical charts: age, sex, histological diagnosis, extent of tongue resection, reconstruction surgical procedures, postoperative ischemic complications, postoperative radiotherapy, and follow-up period. The institutional review board of the Kobe University Hospital approved this retrospective study.
Functional Evaluation During the routine follow-up visits, simple medical inquiries about the postoperative status of patients who underwent hemitongue reconstruction yielded a score range of 0 to 6 points. A single plastic surgeon (K.H.) performed almost all of these clinical assessments.
The Journal of Craniofacial Surgery • Volume 26, Number 1, January 2015
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 26, Number 1, January 2015
Radial Forearm Free Flap Reconstruction
9 women (39.1%). Histological diagnosis was squamous cell carcinoma in all cases. Clinical T stages were as follows: T1, 1 (4.3%); T2, 18 (78.3%); T3, 4 (17.4%). Hemiglossectomy involving the base of the tongue was performed in 4 cases (17.4%). It was limited to the mobile tongue in 19 cases (82.6%). A unilobed radial forearm flap was sutured into the residual tongue tip, with microvascular anastomoses of the radial artery, radial vein, and cephalic vein to the recipient vessels without nerve anastomosis in all cases. There were 2 venous thromboses of the microvascular anastomoses (8.7%). These 2 free flaps were salvaged with a reoperation. No patients underwent postoperative radiotherapy. The mean follow-up period was 85.4 months (range, 60–122 months).
Sequential Changes of Postoperative Status and Reconstructed Tongue Morphology
FIGURE 1. Sequential change of postoperative function. Vertical axis (1–100) represents the percentage of cases acquiring eating, speech, and sensory function = 2 points.
A 2-point scale to evaluate eating function was used. Patients who resumed the same form of diet as was consumed preoperatively were given 2 points. Those who resumed consumption of their preoperative diet but had difficulty eating specific foods (eg, meat or noodles), or they took a very long time to eat, were given 1 point. Those who were unable to consume foods that were in their diet preoperatively were given 0 points. Speech function was evaluated on a 2-point scale. Patients who could talk on the telephone were given 2 points. Those who could talk on the telephone but had difficulty speaking certain words (eg, those with alveolar or velar consonants) were given 1 point. Those who could not talk on the telephone were given 0 points. Sensory function was evaluated on a 2-point scale. Patients who had no complaints were given 2 points. Those who had difficulty eating a hot diet or who bit the flap were given 1 point. Those who could not eat a hot diet and often bit the flap were given 0 points. Sequential changes in postoperative status were retrospectively analyzed. We assessed morphological alterations of the reconstructed tongues by reviewing clinical photographs.
Statistical Analysis Fisher exact test was used to identify significant associations among categorical values. Statistical significance was accepted at P < 0.05, and all calculations were performed using SPSS version 15.0 (SPSS, Chicago, IL).
RESULTS
TABLE 2. Associations With Postoperative Status (Over 5 Points) at 5 Years or Greater Postoperatively No. Cases (%)
Postoperative Status ≤5 (%)
Age, y
At the time of surgery, the mean age of the 23 study subjects was 57 years (range, 33–71 years). There were 14 men (60.9%) and TABLE 1. Passage of Time and Their Associations With Postoperative Status (Over 5 Points) No. Cases Acquiring Postoperative Status ⩽5 (%) 3y ≥5 y
DISCUSSION This study investigated the long-term change in the postoperative status of patients who underwent RFFF reconstruction after hemiglossectomy. It revealed sequential improvement. Although previous long-term follow-up studies have assessed functional outcome of the neotongue, there remained some issues, such as the heterogeneity of study population and the duration of the follow-up period. In 1 report, the functional outcomes in patients
Parameter
Population
1y
Postoperative status improved sequentially. At 1 year after surgery, 21 patients (91.3%) could partake of the same type of diet as they had preoperatively, and all patients could talk on the telephone. While eating and speech function gradually improved, the extent of sensory function improvement lagged behind (Fig. 1). Eight patients (34.8%) had difficulty eating a hot diet or had bitten the flap throughout the follow-up period. At 5 years or longer after surgery, 6 patients (26.1%) were given 4 postoperative status points, 8 (34.8%) were given 5 points, and 9 (39.1%) were assigned 6 points. Statistical differences were analyzed between the patients who were given less than 4 points and those who rated more than 5 points. A significant improvement was found between 1 and 5 years after surgery (P = 0.007), but not between 1 and 3 years (P = 0.075) or 3 and 5 years (P = 0.530) (Table 1). No relation was found between age (P = 0.245), sex (P = 0.643), extent of resection (P = 0.270), or venous thrombosis (P = 1.000) (Table 2). Morphological alterations of reconstructed tongues are shown in Figure 2. The furrows in 2 reconstructed tongues gradually disappeared, which probably reflected the sequential decrease in flap volume (Figs. 2A–D). Morphological changes were not recognized in other flaps during the long-term follow-up periods. Representative cases are shown in Figures 2E–H.
7 (30.4) 14 (60.9) 17 (73.9)
P 0.075 0.007 0.530
≤59 ≥60 Sex Male Female Extent of resection Mobile tongue Mobile tongue and base of tongue Venous thrombosis − +
P 0.245
10 (43.5) 13 (56.5)
70.0 76.9
14 (60.9) 9 (39.1)
79.0 66.7
19 (82.6) 4 (17.4)
79.0 50.0
21 (91.3) 2 (8.7)
71.0 100.0
0.643
0.270
1.000
© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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Akashi et al
The Journal of Craniofacial Surgery • Volume 26, Number 1, January 2015
FIGURE 2. Long-term morphological alterations in the reconstructed tongue. (A–D) Note that the furrows in the flaps disappeared sequentially. A and B, A 42-year-old man at 3 years after surgery (A) and at 5 years (B). C and D, A 47-year-old woman 1 year after surgery (C) and at 8 years (D). E–H, A 70-year-old man at 2 years after surgery (E) and at 5 years (F). A 63-year-old woman 3 years after surgery (F) and at 7 years (H). They exhibited few flap volume changes during this long-term period.
who underwent free flap reconstruction following hemiglossectomy and subtotal and total glossectomy were evaluated with the same modalities.7 The modalities for evaluating the functional outcome in patients who undergo subtotal or total glossectomy should not be applied to those who undergo hemiglossectomy, because the residual tongue following ablation plays critical roles in postoperative function. Various modalities have been applied to evaluate function of the postoperative tongue in patients who have undergone free flap reconstruction (eg, speech intelligibility assessment by speech therapists, swallowing assessment by video-fluoroscopic images, sensory function assessment by 2-point discrimination test).5,6,10 These studies have provided important information, but the examinations cannot be performed routinely during the practical follow-up of hemiglossectomy patients. We evaluated such patients postoperatively with simple medical inquiries, emphasizing their ability to talk on the telephone, which is thought to reflect patients’ speech function in daily life. Questionnaires about this ability are generally included in the applicable methods to evaluate quality of life (QOL), such as the European Organization for Research and Treatment of Cancer Quality of Life Core Questionnaire and Head and Neck Module.11 We also took into account the ability to partake of the same type of diet as was consumed before the operation. This factor was chosen because eating includes mastication and deglutition, which
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are influenced by the patient’s age and whether he/she is dentate or edentate. In a previous study, functions that included swallowing were usually at their worst after cancer treatment, although 1 year postoperatively, almost all patients were consuming a socially acceptable diet.12 In our study, a single patient was unable to consume the same diet as before the surgery at 1 year after surgery but experienced improved eating function sequentially during the 5 years postoperatively, as was seen in all of the other patients (Fig. 1). Conversely, all patients could talk on the telephone 1 year after surgery, and speech improvement, based on our assessment modality, was almost complete at 3 years (Fig. 1). Hsiao et al,5 in the comparative study between primary closure and RFFF reconstruction after hemiglossectomy, reported that the nonfunctional flap added bulk, improving pharyngeal clearance by maintaining the tongue-to-mouth roof contact that was necessary for the swallowing process. It also, however, hindered articulation by restricting mobility of the residual tongue. Although our speech assessment may be more lenient than that of Hsiao et al, the ability to talk on the telephone is considered acceptable for the neotongue. Because acquisition of eating function as well as speech function is required for tongue reconstruction, pliable tissue transfer that does not restrict residual tongue mobility is needed. Sequential improvement of postoperative status in our patients was considered to be due to the pliability of the RFFF. We also evaluated the difficulty of consuming a hot diet and flap biting as parameters of sensory impairment. Whereas there was gradual improvement of sensory function during the 5 years after surgery, the percentage of patients given 2 points of sensory function was lower than ones of eating and speech functions. Previous studies revealed that sensory-innervated flaps for intraoral reconstruction allowed better and faster recovery of sensation than noninnervated flaps.13,14 It is also known that noninnervated flaps eventually may recover sensation through peripheral and recipient bed axonal sprouting, although there is no complete recovery over the entire flap.15,16 Loewen et al10 reported that patients who underwent innervated RFFF reconstruction of the tongue were able to identify cold more accurately than hot. A decrease or loss in protective sensation and pain perception on the free flap may cause a burn as well as flap bites. Flap bites might reflect not only sensory impairment but also bulkiness of the flap or disturbed coordination of mastication.17 Some longitudinal studies to measure changes in QOL in patients with head and neck cancer have been carried out. Rogers et al18 reported that patients tended to emphasize speech, chewing, and swallowing more than other evaluation items (including pain and appearance) at 12 months after surgery. Infante-Cossio et al19 performed a long-term prospective study that included QOL data of 69 patients with oral and oropharyngeal carcinoma. Data were obtained prior to treatment and 1 and 3 years after treatment initiation. They noted that most of the parameters worsened significantly after treatment and during the first year and then gradually improved. At 3 years postoperatively, only a few parameters had not returned to the values before beginning treatment. They concluded that most of the benefit with regard to QOL was acquired during the first years because no further dynamic of QOL was found after the first year of treatment because of tolerance mechanisms over the course of the disease.20 On the other hand, Joo et al21 reported a significant positive correlation between postoperative irradiation and RFFF volume changes estimated by computed tomography or magnetic resonance imaging 3 months to 5 years after surgery—but not 3 months to 1 year or 3 months to 3 years. They recommended overcorrection with 40% larger RFFF volume than the actual defect because the computerdetermined postoperative volume changed by 42.7% between 3 months and 5 years. They noted that the percentage volume of the reconstructed radial forearm flap changed by 15.4% to 75.5% between 3 months and 5 years. In our cases, morphological changes © 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
The Journal of Craniofacial Surgery • Volume 26, Number 1, January 2015
were small except for 2 flaps that exhibited disappearance of the furrows, as shown in Figures 2A–D. The maintenance of flap volume may be explained by the lack of irradiation in all of our patients. Because our study revealed gradual changes in postoperative status, reconstructive surgeons should follow up for as long as possible to evaluate outcomes in their patients who undergo free flap reconstruction. The free anterolateral thigh perforator flap has been considered an alternative to RFFF for head and neck reconstruction. It has become popular nowadays because it leaves less donor-site morbidity.22 Comparison studies between the RFFF and anterolateral thigh flap have been carried out.23–25 Although they found no significant differences in speech or swallowing between the 2 groups, patients with the free anterolateral thigh flaps had better QOL scores, including appearance among others.25 Long-term follow-up regarding changes in the flap volume or sequential atrophy of the free anterolateral thigh flap is reported in a few studies.26 We have used RFFF as a first-choice flap following hemiglossectomy because it is anatomically constant, it has a long vascular pedicle, it is easy to harvest, and (especially) the skin flap has a pliability that cannot be gained from other tissues. Our results, which showed that the postoperative status of patients improved sequentially, certainly reflect the continuous pliability of this flap, which does not limit the mobility of the residual tongue. Based on their experience, Li et al25 recommended that the free anterolateral thigh flap be used for large defects during head and neck reconstruction. There were some limitations of the study. The retrospective nature and small sample size were problematic. Also, technical examinations (eg, functional assessment by a speech therapist, evaluation of swallowing with video fluoroscopy) were not performed. Our assessment of postoperative status in patients who underwent reconstructive free flap transfer after hemiglossectomy comprised the use of questionnaires that were simpler than those previously reported.18–20 Our evaluation modality may be adequate for practical evaluation during routine follow-up of hemiglossectomy patients but not for clinical research. Also, the postoperative status of total glossectomy patients undergoing free flap reconstruction should be evaluated with a more distinctive method because their postoperative functions are worse than those of hemiglossectomy patients. A prospective investigation with the evaluation modality introduced in the present study should be conducted to confirm the validity of free flap reconstruction following hemiglossectomy. ACKNOWLEDGMENTS The authors thank S. Tahara in the Department of Plastic Surgery, Japanese Red Cross Kobe Hospital; S. Yokoo in the Department of Stomatology and Maxillofacial Surgery, Gunma University Graduate School of Medicine; and doctors in the Departments of Oral and Maxillofacial Surgery and Otolaryngology–Head and Neck Surgery, Kobe University Graduate School of Medicine.
REFERENCES 1. Brown JS, Rogers SN, Lowe D. A comparison of tongue and soft palate squamous cell carcinoma treated by primary surgery in terms of survival and quality of life outcomes. Int J Oral Maxillofac Surg 2006;35:208–214 2. Kimata Y, Sakuraba M, Hishinuma S, et al. Analysis of the relations between the shape of the reconstructed tongue and postoperative functions after subtotal or total glossectomy. Laryngoscope 2003;113:905–909 3. Rhemrev R, Rakhorst HA, Zuidam JM, et al. Long-term functional outcome and satisfaction after radial forearm free flap reconstructions of intraoral malignancy resections. J Plast Reconstr Aesthet Surg 2007;60:588–592 4. Urken ML, Biller HF. A new bilobed design for the sensate radial forearm flap to preserve tongue mobility following significant glossectomy. Arch Otolaryngol Head Neck Surg 1994;120:26–31
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5. Hsiao HT, Leu YS, Lin CC. Primary closure versus radial forearm flap reconstruction after hemiglossectomy: functional assessment of swallowing and speech. Ann Plast Surg 2002;49:612–616 6. Joo YH, Hwang SH, Park JO, et al. Functional outcome after partial glossectomy with reconstruction using radial forearm free flap. Auris Nasus Larynx 2013;40:303–307 7. Engel H, Huang JJ, Lin CY, et al. A strategic approach for tongue reconstruction to achieve predictable and improved functional and aesthetic outcomes. Plast Reconstr Surg 2010;126:1967–1977 8. Yun IS, Lee DW, Lee WJ, et al. Correlation of neotongue volume changes with functional outcomes after long-term follow-up of total glossectomy. J Craniofac Surg 2010;21:111–116 9. Hara I, Gellrich NC, Düker J, et al. Evaluation of swallowing function after intraoral soft tissue reconstruction with microvascular free flaps. Int J Oral Maxillofac Surg 2003;32:593–599 10. Loewen IJ, Boliek CA, Harris J, et al. Oral sensation and function: a comparison of patients with innervated radial forearm free flap reconstruction to healthy matched controls. Head Neck 2010;32:85–95 11. Bjordal K, Hammerlid E, Ahlner-Elmqvist M, et al. Quality of life in head and neck cancer patients: validation of the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire–H&N35. J Clin Oncol 1999;17:1008–1019 12. Markkanen-Leppänen M, Isotalo E, Mäkitie AA, et al. Swallowing after free-flap reconstruction in patients with oral and pharyngeal cancer. Oral Oncol 2006;42:501–509 13. Urken ML, Weinberg H, Vickery C, et al. The neurofasciocutaneous radial forearm flap in head and neck reconstruction: a preliminary report. Laryngoscope 1990;100:161–173 14. Katou F, Shirai N, Kamakura S, et al. Intraoral reconstruction with innervated forearm flap: a comparison of sensibility and reinnervation in innervated versus noninnervated forearm flap. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1995;80:638–644 15. Shindo ML, Sinha UK, Rice DH. Sensory recovery in noninnervated free flaps for head and neck reconstruction. Laryngoscope 1995;105:1290–1293 16. Vriens JP, Acosta R, Soutar DS, et al. Recovery of sensation in the radial forearm free flap in oral reconstruction. Plast Reconstr Surg 1996;98:649–656 17. Kapur KK, Garrett NR, Fischer E. Effects of anaesthesia of human oral structures on masticatory performance and food particle size distribution. Arch Oral Biol 1990;35:397–403 18. Rogers SN, Laher SH, Overend L, et al. Importance-rating using the University of Washington quality of life questionnaire in patients treated by primary surgery for oral and oro-pharyngeal cancer. J Craniomaxillofac Surg 2002;30:125–132 19. Infante-Cossio P, Torres-Carranza E, Cayuela A, et al. Impact of treatment on quality of life for oral and oropharyngeal carcinoma. Int J Oral Maxillofac Surg 2009;38:1052–1058 20. Klug C, Neuburg J, Glaser C, et al. Quality of life 2–10 years after combined treatment for advanced oral and oropharyngeal cancer. Int J Oral Maxillofac Surg 2002;31:664–669 21. Joo YH, Hwang SH, Sun DI, et al. Assessment of volume changes of radial forearm free flaps in head and neck cancer: long-term results. Oral Oncol 2011;47:72–75 22. Wei FC, Jain V, Celik N, et al. Have we found an ideal soft-tissue flap? An experience with 672 anterolateral thigh flaps. Plast Reconstr Surg 2002;109:2219–2226; discussion 2227–2230 23. Hsiao HT, Leu YS, Liu CJ, et al. Radial forearm versus anterolateral thigh flap reconstruction after hemiglossectomy: functional assessment of swallowing and speech. J Reconstr Microsurg 2008;24:85–88 24. de Vicente JC, de Villalaín L, Torre A, et al. Microvascular free tissue transfer for tongue reconstruction after hemiglossectomy: a functional assessment of radial forearm versus anterolateral thigh flap. J Oral Maxillofac Surg 2008;66:2270–2275 25. Li W, Xu Z, Liu F, et al. Vascularized free forearm flap versus free anterolateral thigh perforator flaps for reconstruction in patients with head and neck cancer: assessment of quality of life. Head Neck 2013;35:1808–1813 26. Yamaguchi K, Kimata Y, Onoda S, et al. Quantitative analysis of free flap volume changes in head and neck reconstruction. Head Neck 2012;34:1403–1407
© 2014 Mutaz B. Habal, MD
Copyright © 2014 Mutaz B. Habal, MD. Unauthorized reproduction of this article is prohibited.
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